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In a similar role to its namesake, it is used to gather electronic intelligence, and its primary role is to stay hidden while safely gathering such intelligence, not to charge into battle, as that would invariably be an irreversibly fatal tactic, due to its light weapons and armor. Because of its tactical value and potential to change the outcome of any given combat situation, every UNSC battlegroup has at least one Prowler assigned to its ranks.[9]

The Prowler's only combat role, beside active combat monitoring and recording, is discreetly laying minefields of stealthed nuclear HORNET Mines in orbital regions. Enemy ships that unknowingly enter these minefields can be destroyed by a single prowler, allowing the remainder of the UNSC forces to move in and finish off the survivors with MAC strikes and Archer missiles. This stratagem allowed Battle Group Stalingrad to wage a short but devastating battle against the Covenant at Onyx, destroying significantly more ships than their own number, an extremely rare outcome among UNSC-Covenant engagements.

SPARTAN-II Gray Team was able to pilot a Prowler, meaning a Prowler could be piloted by a crew of only three people.

The UNSC Wink of an Eye possessed Active camouflage systems, which were not common among UNSC or Covenant starships. The technology was most likely experimental, since the camouflage could not keep up with the constantly changing atmosphere of the gas giant Viperidae. Such a system was also used by the UNSC Dusk, during the Battle of Onyx, but bizarrely not described as being used during the Covenant Schism at Installation 05, despite there being five times as many, or more Covenant ships than at Onyx.

Unlike other UNSC ships which are rectangular, long, and narrow in design, the UNSC Prowler is rather wide and has curved, wing-like extensions on its hull.